Comparative and phylogenetic analysis of a novel family of Enterobacteriaceae-associated genomic islands that share a conserved excision/integration module

Abstract

Genomic Islands (GIs) are DNA regions acquired through horizontal gene transfer that encode advantageous traits for bacteria. Many GIs harbor genes that encode the molecular machinery required for their excision from the bacterial chromosome. Notably, the excision/integration dynamics of GIs may modulate the virulence of some pathogens. Here, we report a novel family of GIs found in plant and animal Enterobacteriaceae pathogens that share genes with those found in ROD21, a pathogenicity island whose excision is involved in the virulence of Salmonella enterica serovar Enteritidis. In these GIs we identified a conserved set of genes that includes an excision/integration module, suggesting that they are excisable. Indeed, we found that GIs within carbapenem-resistant Klebsiella pneumoniae ST258 KP35 and enteropathogenic Escherichia coli O127:H6 E2348/69 are excised from the bacterial genome. In addition to putative virulence factors, these GIs encode conjugative transfer-related proteins and short and full-length homologues of the global transcriptional regulator H-NS. Phylogenetic analyses suggest that the identified GIs likely originated in phytopathogenic bacteria. Taken together, our findings indicate that these GIs are excisable and may play a role in bacterial interactions with their hosts.

Pathogenicity island excision during an infection by Salmonella enterica serovar Enteritidis is required for crossing the intestinal epithelial barrier in mice to cause systemic infection

“…Several members of Enterobacteriaceae family have on their chromosome a type of excisable PAIs denominated ROD21-like islands [26,27]. This is the case of Salmonella sp (ROD21 and SPI-7) [23], Escherichia coli UPEC (PAI I536, PAI II536, and PAI V536) [36], Klebsiella pneumoniae (GIE492) [37], Vibrio cholera (VPI-2 VSP-I and VSP-I) [38], and Pectobacterium atrosepticum (HAI2) [39].…”

“…Previous studies with S. Enteritidis-ΔDRSΔint have suggested that the impairment of ROD21 excision can modulate the expression of genes within ROD21 [27]. Therefore, we evaluated whether S. Enteritidis-ΔintΔrdf strain also showed an altered gene expression, equivalent to S. Enteritidis-ΔDRSΔint, and whether impairment of ROD21 excision affects the transcription of genes within ROD21 and genes in other pathogenicity islands that are required for invasion of epithelial cells and the establishment of a systemic infection in mice.…”

“…and S. Antatum [27]. ROD21-like islands has also been found in other members of the Enterobacteriaceae family that include Escherichia coli ETEC-2265, Klebsiella pneumoniae 30684, Klebsiella oxytoca AR0147 and Pectobacterium atrosepticum SCRI1043 [27].…”

“…This latter protein is involved in DNA organization and contributes to the replication, segregation, repair and expression of the bacterial chromosome [30][31][32]. Previous in vitro studies have shown that strains unable to excise ROD21 displayed altered expression of the genes located in this PAI [27,33], suggesting that excision might also regulate gene transcription. Even though the relationship between PAIs excision and virulence has not been completely elucidated, previous reports suggest that strains of S. Enteritidis that are unable to excise ROD21 have a reduced capacity to colonize the liver and spleen of mice, as compared to the WT strain [33].…”

Genome analysis of a wild rumen bacterium Enterobacter aerogenes LU2 - a novel bio-based succinic acid producer

“…These regions may encode numerous beneficial traits for bacteria and thus have an influence on better adaptation of microorganisms to changing environmental conditions. Due to the gene content, these regions can be divided into pathogenicity, metabolic, fitness, symbiosis and resistance islands and can be distinguished from the host genome based on different nucleotide compositions, including IS fragments, anomalous GC content, transposons and tRNA genes 37,38 . To evaluate the genetic diversity of E. aerogenes LU2, the presence of GIs acquired through HGT was identified using the IslandViewer 4 platform and the IslandPath-DIMOB, SIGI-HMM, and IslandPick prediction methods (Additional file 1) 39 .…”